Organic anions in the rhizosphere of Al-tolerant and Al-sensitive wheat lines grown in an acid soil in controlled and field environments
C. R. Schefe A D , M. Watt B , W. J. Slattery C and P. M. Mele AA Primary Industries Research Victoria (PIRVic), Department of Primary Industries, Rutherglen Centre, RMB 1145, Rutherglen, Vic. 3685, Australia.
B CSIRO Plant Industry, GPO Box 1600, Canberra, ACT 2601, Australia.
C Australian Greenhouse Office, GPO Box 621, Canberra, ACT 2601, Australia.
D Corresponding author. Email: cassandra.schefe@dpi.vic.gov.au
Australian Journal of Soil Research 46(3) 257-264 https://doi.org/10.1071/SR07139
Submitted: 19 September 2007 Accepted: 13 February 2008 Published: 1 May 2008
Abstract
Several sampling methods were investigated for the quantification of organic anions in the rhizosphere of Al-tolerant (ET8) and Al-sensitive (ES8) wheat plants in soil systems. Controlled environment studies used anion exchange membranes to collect rhizosphere organic anions (from root tips and mature regions of nodal roots) from ET8 and ES8 plants at the 6-leaf stage in a glasshouse environment. Using the anion exchange membranes, a selection of organic anions were detected on the tips and mature regions of roots, with ET8 and ES8 having similar rhizosphere organic anion profiles. The field experiment used 2 established methods of organic anion collection: rhizosphere soil and root washings. The ET8 and ES8 wheat lines had similar levels of organic anions, including malate, in the rhizosphere (using soil shaken from roots and root washings) at 3 sampling times (4 and 6 leaves, and flowering). The rhizosphere organic anions differed significantly from the bulk soil, with the concentration and range of organic anions in the rhizosphere decreasing towards flowering, presumably due to physiological changes in plant and root growth. This study used several techniques to investigate organic anion exudation by roots, with organic anions detected using all techniques. However, technical limitations of these techniques were recognised: (i) the lack of simultaneous exposure of root tips to both the anion exchange membrane and the chemical stimulant, e.g. Al3+; and (ii) the inability to derive the origin of organic anions measured in rhizosphere soil and root washings. The challenge for future soil-based organic anion research is to identify the dominant stress that has triggered an exudation response (i.e. Al toxicity, P deficiency), and to clearly differentiate between plant- and microbial-derived contributions to exudation.
Additional keywords: anion exchange membranes, HPLC, malate, rhizosphere, sorption.
Acknowledgments
This work was funded through the Science, Technology and Innovation (STI) program of the Department of Innovation, Infrastructure and Regional Development (DIIRD), Victoria, and from the GRDC for MW. We are grateful to Dr Caixan Tang of La Trobe University for providing the seed, Greg Codes for the access to the field site, and Dr Maartin Hens, CSIRO Plant Industry, for assistance with the anion-exchange membrane method. Thanks also to Dr Erik Veneklaas, University of Western Australia, for advice on collecting root leachates and reviewing the manuscript, and Drs Matt Denton and Kirsten Barlow, Department of Primary Industries, Victoria, and Dr Alan Richardson, CSIRO Plant Industry for reviewing the manuscript.
Basu U,
Godbold D, Taylor GJ
(1994) Aluminum resistance in Triticum aestivum associated with enhanced exudation of malate. Journal of Plant Physiology 144, 747–753.
Cieśliński G,
Van Rees KCJ,
Szmigielska AM,
Krishnamurti GSR, Huang PM
(1998) Low-molecular-weight organic acids in rhizosphere soils of durum wheat and their effect on cadmium bioaccumulation. Plant and Soil 203, 109–117.
| Crossref | GoogleScholarGoogle Scholar |
Delhaize E,
Ryan PR, Randall PJ
(1993) Aluminium tolerance in wheat (Triticum aestivum L.) II. Aluminium-stimulated excretion of malic acid from root apices. Plant Physiology 103, 695–702.
| PubMed |
Delhaize E,
Ryan PR,
Hebb DM,
Yamamoto Y,
Sasaki T, Matsumoto H
(2004) Engineering high-level aluminum tolerance in barley with the ALMT1 gene. Proceedings of the National Academy of Sciences of the United States of America 101, 15249–15254.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Dinkelaker B,
Römheld V, Marschner H
(1989) Citric acid excretion and precipitation of calcium citrate in the rhizosphere of white lupin (Lupinus albus L.). Plant, Cell & Environment 12, 285–292.
| Crossref | GoogleScholarGoogle Scholar |
Dong D,
Peng X, Yan X
(2004) Organic acid exudation induced by phosphorus deficiency and/or aluminium toxicity in two contrasting soybean genotypes. Physiologia Plantarum 122, 190–199.
| Crossref | GoogleScholarGoogle Scholar |
Grierson PF
(1992) Organic acids in the rhizosphere of Banskia integrifolia L. f. Plant and Soil 144, 259–265.
| Crossref | GoogleScholarGoogle Scholar |
Jones DL
(1998) Organic acids in the rhizosphere – a critical review. Plant and Soil 205, 25–44.
| Crossref | GoogleScholarGoogle Scholar |
Jones DL,
Darrah PR, Kochian LV
(1996a) Critical evaluation of organic acid mediated iron dissolution in the rhizosphere and its potential role in root iron uptake. Plant and Soil 180, 57–66.
| Crossref | GoogleScholarGoogle Scholar |
Jones DL,
Dennis PG,
Owen AG, van Hees PAW
(2003) Organic acid behaviour in soils – misconceptions and knowledge gaps. Plant and Soil 248, 31–41.
| Crossref | GoogleScholarGoogle Scholar |
Jones DL,
Prabowo AM, Kochian LV
(1996b) Aluminium-organic acid interactions in acid soils II. Influence of solid phase sorption on organic acid-Al complexation and Al rhizotoxicity. Plant and Soil 182, 229–237.
Kataoka T,
Stekelenburg A,
Nakanishi TM,
Delhaize E, Ryan PR
(2002) Several lanthanides activate malate efflux from roots of aluminium-tolerant wheat. Plant, Cell & Environment 25, 453–460.
| Crossref | GoogleScholarGoogle Scholar |
Kerven GL,
Edwards DG,
Asher CJ,
Hallman PS, Kokot S
(1989) Aluminium determination in soil solution II. Short-term colorimetric procedures for the measurement of inorganic aluminium in the presence of organic acid ligands. Australian Journal of Soil Research 27, 91–102.
| Crossref | GoogleScholarGoogle Scholar |
Kinraide TB,
Parker DR, Zobel RW
(2005) Organic acid secretion as a mechanism of aluminum tolerance. A model incorporating the root cortex, epidermis, and the external unstirred layer. Journal of Experimental Botany 56, 1853–1865.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Li XF,
Ma JF, Matsumoto H
(2002) Aluminium-induced secretion of both citrate and malate in rye. Plant and Soil 242, 235–243.
| Crossref | GoogleScholarGoogle Scholar |
Ma JF,
Ryan PR, Delhaize E
(2001) Aluminium tolerance in plants and the complexing role of organic acids. Trends in Plant Science 6, 273–278.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Menzies NW,
Bell LC, Edwards DG
(1991) A simple positive pressure apparatus for the ultra-filtration of soil solution. Communications in Soil Science and Plant Analysis 22, 137–145.
Nian H,
Yang ZM,
Ahn SJ,
Cheng ZJ, Matsumoto H
(2002) A comparative study on the aluminium- and copper-induced organic acid exudation from wheat roots. Physiologia Plantarum 116, 328–335.
| Crossref | GoogleScholarGoogle Scholar |
Pearse SJ,
Veneklaas EJ,
Cawthray G,
Bolland MDA, Lambers H
(2006) Triticum aestivum shows a greater biomass response to a supply of aluminium phosphate than Lupinus albus, despite releasing fewer carboxylates into the rhizosphere. New Phytologist 169, 515–524.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Rengel Z
(2002) Genetic control of root exudation. Plant and Soil 245, 59–70.
| Crossref | GoogleScholarGoogle Scholar |
Ryan PR,
Delhaize E, Jones DL
(2001) Function and mechanism of organic anion exudation from plant roots. Annual Review of Plant Physiology and Plant Molecular Biology 52, 527–560.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ryan PR,
Delhaize E, Randall PJ
(1995) Characterisation of Al-stimulated efflux of malate from the apices of Al-tolerant wheat roots. Planta 196, 103–110.
| Crossref | GoogleScholarGoogle Scholar |
Slattery WJ,
Morrison GR, Coventry DR
(1995) Liming effects on soil exchangeable cations of four soil types in north-eastern Victoria. Australian Journal of Soil Research 33, 277–295.
| Crossref | GoogleScholarGoogle Scholar |
Ström L,
Owen AG,
Godbold DL, Jones DL
(2002) Organic acid mediated P mobilisation in the rhizosphere and uptake by maize roots. Soil Biology & Biochemistry 34, 703–710.
| Crossref | GoogleScholarGoogle Scholar |
Tang C,
Rengel Z,
Abrecht D, Tennant D
(2002) Aluminium-tolerant wheat uses more water and yields higher than aluminium-sensitive one on a sandy soil with subsurface acidity. Field Crops Research 78, 93–103.
| Crossref | GoogleScholarGoogle Scholar |
Veneklaas EJ,
Stevens J,
Cawthray GR,
Turner S,
Grigg AM, Lambers H
(2003) Chickpea and white lupin rhizosphere carboxylates vary with soil properties and enhance phosphorus uptake. Plant and Soil 248, 187–197.
| Crossref | GoogleScholarGoogle Scholar |
Yang J,
Zhang J,
Wang Z,
Zhu Q, Liu L
(2001) Water deficit–induced senescence and its relationship to the remobilization of pre-stored carbon in wheat during grain filling. Agronomy Journal 93, 196–206.